Table Of Content©SociedadEspañoladeMalacología Iberus, 28 (2): 63-72, 2010
NE
Spawn and early development of Atlantic species of
Hypselodoris (Gastropoda: Opisthobranchia)
Puestay desarrollo de especies del género HypselodorisdelAtlántico
nororiental (Gastropoda: Opisthobranchia)
Rita COELHO*’** and Gonzalo CALADO***
Recibidoel23-X-2010.Aceptadoel24-XI-2010
SUMMARY
Despite an existing review of the Atlantic species of the family Chromodorididae (Mol-
lusca: Nudibranchia), little is known about early development patterns of these species
due to the difficulty of collecting data from living animáis. Six species of the genus
Hypselodoris inhabit the Portuguese continental coasts: H. bilineata, H. cantábrico, H.
fontandraui, H. picta, H. tricolorand H. villafranca. This paper is based on new data and
extensive studies made under laboratory conditions and aims to describe several aspects
of their reproduction, namely egg mass type, egg size and colour, duration of embryonic
development and development patterns. The data here obtained and existing developmen-
tal data for Atlantic Hypselodoris from the literature are also compared.
RESUMEN
A pesar de que existe una revisión de las especies atlánticas de la familia Chromodoridi-
dae (Mollusca: Nudibranchia), muy poco se conoce acerca de la biología y patrones de
desarrollo de estas especies debido a la dificultad de obtener datos a partir de ejempla-
res vivos. Seis especies del género Hypselodoris habitan en las costas continentales por-
tuguesas: H. bilineata, H. cantábrico, H. fontandraui, H. picta, H. tricolory H. villafranca.
En el presente trabajo de aportan nuevos datos obtenidos de estudios en condiciones de
laboratorio con el objetivo de describir algunos aspectos de la biología reproductora de
estas especies, como el tipo de puesta, tamaño del huevo y color, duración del desarrollo
embrionario y patrón de desarrollo. Los datos obtenidos en el presente trabajo se (sinteti-
zan y) comparan con los existentes en la bibliografía.
INTRODUCTION
The Family Chromodorididae (Mol- and García-Gómez, 1996) of the At-
lusca: Nudibranchia) comprises one of lantic species ofthe familyChromodori-
the most fantastic coloured Nudibranch didae Bergh, 1891 (Mollusca: Nudi-
groups of the Iberian Peninsula East branchia), studies specifically devoted
coast. Despite a review (Ortea, Valdés to their reproductive biology, from egg
* Instituto Portugués de Malacologia, Zoomarine, E.N. 125, Km 65 Guia; 8201-864Albufeira; Portugal. E-
mail: [email protected]
**CenterofMarineScience-CCMAR,UniversityofAlgarve,Faro, Portugal.
*** Universidade Lusófona de Humanidades e Tecnologías, Av. do Campo Grande, 376
1749-024Lisboa, Portugal.
63
Iberus, 28 (2), 2010
to metamorphosis are absent. General considered, namely egg mass type, egg
data on egg mass shapes, egg size or size and colour, duration of embryonic
egg-to-juvenile periods are scarce, scat- developmentanddevelopmenttype.
tered or absent. Quite often available
data come from one single specimen.
Furthermore, dispersión measures or MATERIALAND METHODS
confidenceintervalsaremostlyabsent.
Like with most aspects of nudi- Specimens studiedwere collected on
branch biology, there is no general rule subtidal surveys using scuba diving in
concerning their life history and life Arrábida (West Coast-38°30' 18" N, 8o
span. Most species seem to live for 55' 18" W) andtheAlgarve (Southcoast-
about one year, although the tropical 37° 00' 08" N, 7o 49' 20" W), Portugal,
Sea haré Dolabella auricularia has been from April 2004 to June 2005. After col-
reported to live for six years in an lection, the animáis were brought to the
aquarium (Hadfield and Switzer- laboratory and placed in closed-circuit
Dunlap, 1984) and the cephalaspidean 40 L aquaria, where water quality was
Philine aperta can live for up to four monitored daily for temperature, pH
years in nature (Lancaster, 1983). On and salinity, and weekly for the pres-
the other hand, there are small nudi- ence ofnitrites, nitrates and phosphates.
branchs, especially those that live and Individuáiswere keptata constanttem-
feed on short-lived cnidarian colonies perature (18±1°C), as similar as possible
which can complete a life cycle in a few to that of their natural environment,
weeks. For example, both the European because egg development timing is
aeolid Tenellia pallida (Alder and known to be strongly affected by tem-
Hancock, 1842) [= T. adspersa (Nord- perature; this parameter was kept con-
mann, 1845)] and the coral-eating tropi- stant in order to make developmental
cal aeolid Cuthona poritophages Rudman, comparisons. Adults ofthe same species
1979 can mature in three weeks (Ras- were kept together and fed with one of
mussen, 1944; Rudman, 1979) and prob- their natural prey Ítems, the corneous
ably die within two or three months. In demosponge Dysideafragilis (Montagu,
the case of these very short-lived 1818), which is very common along the
species, theyneed to complete their life- Portuguesecoasts.
cycle before the colony they live and Egg masses were generally laid on
feed on dies. If they are too slow then the glass walls of the aquaria. The
theywill themselves die from starvation oviposition was considered complete
beforetheycanbreed. when the adult abandoned the egg
Six species of the nudibranch genus mass. Then, the egg masses were care-
Hypselodoris inhabit theAtlantic coast of fully removed from the aquaria, incu-
Portugal (Cervera, Calado, Gavaia, bated individually in 500 Lbeakers at a
Malaquías. Templado, Ballesteros, constant temperature (18°C±1) and
García-Gómez and Megina, 2006): checked periodically until larval hatch-
Hypselodoris billineata (Pruvot-Fol 1953), ing. Extensive observations during
Hypselodoris cantábrica (Bouchet and embryonic development were made
Ortea, 1980), Hypselodoris fontandraui with an optical microscope at regular
(Pruvot-Fol, 1951), Hypselodoris picta periods (4-5 times a day) in the centreof
webbi (D'Orbigny, 1839), Hypselodoris tri- the egg mass, in order to register the
color (Cantraine, 1835), and Hypselodoris main development stages before hatch-
villafranca (Risso, 1818). ing. Daily inspection of all aquaria was
In this paper we report for the first necessary to ensure the measurement of
time data onthe spawnand early devel- zygote diameters before first cleavage
opment of six sympatric Hypselodoris since in these planktotrophic species
species from Portuguese continental initialdevelopmentisveryfast.
coasts maintained under similar labora- The classification followed for
tory conditions. Several aspects were Hypselodoris egg masses is the one pro-
64
COELHOAND CALADO: Spawn and earlydevelopmentofNEAtlanticHypselodoris
Figure 1.EggribbonsofH. bilineata(A),H.pictawebbi(B), andH. villafranca(C). Scalebars,2cm.
Figura 1. PuestadeH. bilineata (A), H. pictawebbi (B)yH.villafranca (C). Escalas,2cm.
posed by Wilson (2002), which deais Hypselodoris spp. egg masses are shaped
exclusivelywith the family Chromodor- like a spiral ribbon attached to the sub-
ididae. According to this author, stratum along one edge and consisting
Hypselodoris egg masses are grouped in of embryos embedded in a gelatinous
the following types: A) fíat egg masses matrix (Fig. 1).
attached to the substratumby thebroad Hypselodoris egg masses found are
side of the ribbon; B) egg masses with a grouped in two types: H. billineata, H.
free edge, shorter or equal than the cantábrica, H.fontandraui, H. picta, H. tri-
attached edge causing the ribbon to color have egg masses corresponding to
slopetoward thecentre orstand upright typeC ofWilson (2002), whereasH. vil-
respectively; C) egg masses with a free lafranca have type A ones. Developmen-
edge, slightly longer or much longer tal characteristics of the studied species
than the attached edge, causing the aresummarizedinTableI.
ribbon to slope away from the centre of H. villafrancaistheonlyspeciesstud-
the spiral or causing ondulations/waves, ied with direct development. All ob-
withanoutwardslope. served eggmasses fromthis specieshad
The criteria used to classify the embryos passing through a suppressed
species larval development were those veliger stage before hatching as benthic
outlined by Thompson (1967, 1976): juveniles. This form of direct develop-
Type 1) planktotrophic development, ment has been categorized by Bonar
with a free veliger stage that can be (1978) as ametamorphic direct develop-
pelagic for an extended period of time ment, which means that this species
and that feeds obligatorily on plankton; does not fully develop into a veligerbe-
Type 2) development with lecitotrophic foreundergoingmetamorphosis.
larvae, with a short-life pelagic veliger All other five Hypselodoris species
that can dispense withplankton feeding studied present a free living plank-
due to their large yolk reserves; type 3) totrophic veliger, which have similar
direct development, without a free developmental characteristics. Despite
pelagiclarvalphase. the differences in egg dimensions (Table
I), hatching times were also very similar
(Fig. 2).
RESULTS Right after complete oviposition we
could often observe two to three differ-
Egg masses produced in the labora- ent stages of development in the same
tory by these nudibranchs are identical spawn. The first part to be released
to those collected in the field. All could show second cleavage (4cells),by
65
9 7
Iberus, 28 (2), 2010
TableI. ComparativetableofdevelopmentalcharacteristicsofspeciesofthegenusHypselodorisofthe
PortugueseCoast,at 18±1°C.Whenappropriate,meanmeasuresaregiven±standarddeviation.
Tabla I. Tabla comparativa de las característicasdeldesarrollo en especies delgénero Hypselodoris en
lascostasportuguesas, a 18±1°C.
3E studied
(m/)i (yL/m) type (days) O)
specimens
range diameter capsule period I
of
diameter per Developmental o
Geogrcphic Capsule Embryonic f, Number
Egg Eggs .2
H.bilineata EasternAtlantic 73.07±7.1 123.16±9.89 1 Planktotrophic 7,75±0,25 139,5±4,4 10
H.cantábrico EasternAtlantic 95.73±8.41 126.96±0.28 1 Planktotrophic 8.25±0.35 161.5±6.0 10
ti.fontandraui EasternAtlantic 86.41±4.10 135.61±22.15 1 Planktotrophic 7.50±0.14 156.9±5.8 10
H.pictawebbi Caribbeanand 171.16±10.52 314.73±41.73 1-2 Planktotrophic 8.04±0.13 219.2±8.3 10
EasternAtlantic
H.tricolor EasternAtlantic 85.65±6.97 147.93±25.74 1 Planktotrophic 7.71±0.1 143.2±2.8 10
EasternAtlantic,
exceptCanary
H. villafranca 243.69±46.06 389.60±45.32 1 Direct 28.00±0.82 515±23 10
Islands.Madeira
andAzores
DUAfjiuiuyyiuup - vdiiduit?. imit:iiduuimly
Mean
Mean±SE
XMean±SD
Species
Figure 2- Time hatching duration for all planktotrophic Hypselodoris species studied (HB= H.
bilineata HT= H. tricolor HF=H.fontandraui HC=H. cantábrica HP= H.picta).
, , , ,
Figura 2- Tiempo hasta la eclosión de las especiesplAde Hypselodoris estudiadas (HB= H. bilineata,
HT= H. tricolor, HF= H. fontandraui, HC= H. cantábrica, HP= Hypselodorispicta!
ÓÓ
COELHOAND CALADO: Spawn andearlydevelopment ofNEAtlanticHypselodoris
Table II. OverView and timing ofembryonic development in species ofthe genus Hypselodoris of
thePortugueseCoast, at 18±1°C.
Tabla II. Resumen de la cronología del desarrollo embrionario desarrollo en especies delgénero
Hypselodorisenlascostasportuguesas, a 18±1°C.
'Z' J hours)
J hours)
(hours) (hours) (hours) i
C1lseatvage 2Clenavdage 3Cleravdage (Mhórouulras) (Blháostuurlsa) -<10s1 cV<aS=/j>)» sVteagleifdgaeysr; (Hadtacyhisn;g
H.bilineata 2h 4h 7h 12h 17h Id;14h 2d;19h 5d;20h 7d;18h
H.cantábrico 2h 4h 8h 13h 20h Id;18h 3d;13h 6d;4h 8d;Ih
H.fontandraui 2h 5h 7h 14h 17h Id;15h 2d;17h 6d;lh 7d;12h
H.picta 2h 3h30' 8h 13h 25h Id;21h 3d;18h 6d;6h 8d;6h
H.tricolor 2h 5h 7h 13h 20h Id;14h 2d;19h 6d—;lh 7d;17h
H. villafranca 2h 24h 42h 72h 168h 9d lid;6h 28d
the time the later eggs were emerging time. Juveniles ofHypselodoris villafranca
from the oviduct, still undivided. The are dorid-like in shape. They measure
stages from mórula to blástula were 515±23 pm in length at hatching and
observed during day 0 for all species present a translucentmantle withbright
exceptH. villafranca. yellow random spots. A structural spic-
Gastrulation was seen during day 1 ular-like network can be seen in the
exceptinH. villafranca,whereitwasonly mantle tissue. This network is main-
observed by day 9. Only after day 5/6 tained in adults of many dorids but is
could we designate larvae as true lost in most chromodorids. No eyes or
veligers because a shell and a bilobed rhinophores buds are visible (Fig. 4).
velumcouldbeclearlyseen. Inthisstage During the first 10-12h post-hatching
veligerswerevery active inside the cap- juveniles crawl on top of the gelatinous
sules. Duration ofthe embryonic period matrix of the spawn, sometimes
fromegg to gastrula ofall species ispre- seemingtograzeonit.
sented in Figure 3. The hatching stage In Table III we summarise the avail-
occurred between days 7 and 8 after able information on the developmental
ovipositionforplanktotrophicspecies. characteristicsofthestudiedspecies.
The general pattern of cleavage,
gastrulation and early embryogenesis of
all species examined is typical of that DISCUSSION
described for other Opisthobranch gas-
tropods (Gohar and Solimán, In this study several aspects of the
1967a,b,c). The main embryonic devel- spawn and development of six species
opment stages and timings are pre- ofthegenusHypselodoris Stimpson, 1855
sented in Table II. Most planktotrophic aredescribed.
species ofHypselodoris studied present a The type of egg mass presented by
veliger with a size within the range of H. villafranca isquiteremarkable, sinceit
139.5pmto 161.5pm. Exceptionismade istoourknowledgethefirstobservation
forHypselodorispicta zvebbiveligerwhich of direct development among chro-
reaches 219.2 pm in length at hatching modorids.
67
,
Iberus 28 (2), 2010
3
"
H. villafranca
I
-
H. tricolor ar
|
-
i
H.picta
|
-
H.fontandraui
|0 1
-
H. cantábrica i
|
-
H. bilineata i
|
100 200 300 400 300 600
Hours
IstCleavage 3rdCleavage Blástula
j j
^
2ndCleavage Mórula Gastrula
i I
Figure3. EmbryonicperioddurationfromeggtogastrulainallspeciesstudiedofHypselodoris.
Figura3. Duracióndeldesarrolloembrionariohastaelestadodegastrula.
Concerning egg size, the mean to 171 pm in H. pida webbi (average
diameterinH. bilineata,H. cantábrica,H. adult length lOOmm). The latter is the
fontandraui and H. tricolor is below 100 largestplanktotrophicegg size reported
pm, within the range reported for most so far among nudibranchs (see Todd,
Nudibranchia species (Hadfield and Lambert and Davies, 2001 for a
Miller, 1987) and consistent with the review). Clearly the amount of energy
planktotrophy exhibited. Egg and packed into each ovum is very differ-
capsule sizes are classically considered ent. Nevertheless, survivorship and
to be good predictors of development time to competence in these larvae
type (Hadfieldand Switzer-Dunlap, remains unknown. The difference in
1984) and used for comparative pur- hatching time between species with
poses (Hadfieldand Miller, 1987). In planktotrophic larvae and the one with
the case of the Atlantic Hypselodoris direct development is certainly due to
pida, however, this extrapolation developmentalconstraints. Evenso, the
clearly predicts direct development, as total egg-to-juvenile period is generally
in H. villafranca, but fails to predict longer and variable in the plank-
pelagic-lecithotrophy which should be totrophic strategy since it is dependent
the case ofH. pida webbi if one follows of an external source of energy to
Hadfield and Switzer-Dunlap's undergo metamorphosis (Todd, 1983;
(1984) predictions. The same situation Havenhand, 1993).
was reported by Thompson (1967) for One of the reasons for supporting
Archidoris pseudoargus, a planktotrophic egg size with capsule size data, in order
developer whose eggs are 170 pm in to have a more accurate development
diameter. A free-swimming, plank- extrapolation (ClarkandJensen, 1981;
totrophic veliger can emerge from eggs Hadfield and Miller, 1987) is the fact
ofverydifferentsizes, from73pminH. thattherearespecieswithlecithotrophic
bilineata (average adult length 30mm), or even direct development although
68
COELHOAND CALADO: Spawn and earlydevelopment ofNEAdanticHypselodoris
Figure4. NewlyhatchedjuvenileofH. villafranca.
Figura4.JuvenilreciéneclosionadodeH.villafranca.
having small eggs. This is common The development from gastrula
among Sacoglossa species as stated by stage to veliger, with all typical struc-
Jensen (2001). The situation can be turespresentlastsbetween 102-107h.
explained based on the presence of It is obvious that Opisthobranch
albumen, an intracapsular substance life-cycle and developmental strategies
rich in proteins and very common in are inextricably linked to adult food
Opisthobranchia spawns (Clark and specificity. Species that feed on tran-
Jensen, 1981) and the existence ofextra- sient food organisms are usually small
capsular yolk in some species, which and present a short life cycle, with a
gives additional nutritional support for veryrapid embryonic development. On
embryos, larvae and juveniles (Marín the other hand, species, like the
andRos, 1993). Hypseloris here presented, that depend
All studied species show a holoblas- on large long-living colonies such as
tic and spiral cleavage, typical of the sponges, are often bigger in size and
Gastropoda group (Biggelaar and have longer life cycles with slower
Haszprunar, 1996). With the exception embryonic development (Rudmanand
of H. villafranca with its slower direct Willan, 1998).
development, all species reach mórula Although some developmental
stage 12-14h after oviposition and gas- timetables have been reported for a
trula stage before the 48h mark. Both number of opisthobranch species, it is
planktotrophic and direct development often difficult to use them to make com-
species gastrulate by emboly, as parisons due to uncontrolled husbandry
described for Dendrodoris and Chro- conditions orsevere differences inwater
modoris by Gohar and Solimán culture temperature, which is known to
(1967a,b) and for Platydoris by Solimán, be one of the key factors affecting
(1978). embryonicdevelopment.
69
Iberus, 28 (2), 2010
Table III. Summary ofdevelopmental characteristics ofAtlantic species ofthe genus Hypselodoris
fromavailableliteratureandpresentstudy.
SPECIES Typeofeggmass Eggmasscolor Eggmasswidth(mm) No.ofspecimens Typeofcapsule
H.bilineata 1 whorlspiralribbon White 3 . .
Spiralribbon White - - -
3whorlsribbon Red-orange 5 1 -
2Whorlsspiralribbon White 4
2-2,5WhorlsSpiralribbon White 3 7 Oval
2Whorlsspiralribbon White 8 Spherical
H.cantábrico 4whorlsspiralribbon White - - -
Spiralribbon White - 1 Oval
Spiralribbon White 1
4whorlsspiralribbon White 10 Oval
H.fontandraui Spiralribbon White - - -
Spiralribbon White - - -
Spiralribbon White - 1 -
2Whorlsspiralribbon White - 10 -
H.pictawebbi Wavedspiralribbon Red-orange 6 - -
Smoothlywavedspiralribbon Orange - - -
5Whorlswavedspiralribbon 10 1 -
4Whorlswavedspiralribbon Pink-orange - - -
H.tricolor 3whorlsspiralribbon White 2 - -
Spiralribbon White - 3 Spherical
2.5WhorlsSpiralribbon White 3 5 -
2Whorlsspiralribbon White - - -
H. villafranca 2Whorlsspiralribbon Orange 2.5mm - -
Spiralribbon Orange - 2 Ovalorspherical
1 whorlspiralribbon Orange Spherical
The studies on development pre- patternanddespitedifferencesineggsize
sented by Martínez-Pita, Sánchez- nodifferencesareregisteredforhatching
Espanñaand García (2006) on species times.Hypselodorispictawebbipresentsthe
of Polycera, conducted at 19°C, report biggestveliger(219.2±8.3pm)butthissize
similarembryonicstagetimingstothose discrepancy with other planktotrophic
presented for planktotrophic species of speciesseemstobemorerelatedtoadult
Hypselodoris in the current study. size (approximately lOOmmlength) than
Yonow (1996) cultured Acteon tornatilis toanydevelopmentalpattern.Neverthe-
at 12°C water temperature and noted less,survivorshipandtimetocompetence
that the 4-cell stage was reached about intheselarvaeremainsunknown.
24h after oviposition and the gastrula When hatching, morphological
stage within 4.9-6d. Although there are resemblance of Hypselodoris villafranca
no significant differences in develop- crawlingjuveniles to adult specimens is
ment pattern between compared very limited and no rhinophores are
species, these last data report a much visible. The crawling behaviour that the
slower embryonic development than juvenile exhibits for 10-12hontop ofthe
our study, which is probably due to the gelatinousmatrixofthe spawn, seeming
6°Cdifferenceinwatertemperature. to graze on it, leads us to think that
AllHypselodorisplanktotrophicspecies matrix nutrients are not only important
exhibit a similar embryonic growth during embryonic development but
70
COELHOAND CALADO: Spawn andearlydevelopmentofNEAtlanticHypselodoris
TablaIII. Resumen delasprincipalesaspectosdeldesarrollodelasespeciesatlánticasdelgénero Hypse-
lodorisobtenidasapartirdelabibliografíaydelpresenteestudio.
Capsulediameterijjm) No.ofeggspercapsule Eggdiameter(¡ám) Embryonicperiodindays SOURCE
100-120 _ 79-109 . Orteaetal(1996)
110-120 1 - - GarcíaGómez(2002)
- 175-208 - BouchetandOrtea(1980)
120 1 11 (18-20°C) Gantes(1962)
158(±3,5)l 1 85-100 9(21°C) Sánchez-Tocinoetal(2007)
100-133 1 67-100 7.75±0.25 CurrentStudy
- - 95-125 7(22°C) Orteaetal[1996)
90-140 1 - - GardaGoméz(2002)
95-125 1 80-85 Sánchez-Tocinoe/a/(2007)
117-144 1 75-120 8.25±0.35 CurrentStudy
150-180 - 110-120 - Orteaetal.(1996)
150-180 1 - - Garcia-Gómez (2002)
145-180 1 110 13(18°C) Sánchez-Tocinoetal.(2007)
95-233 1 80-100 7.50±0.14 CurrentStudy
- - 175-208 - Orteae/o/(1996)
160-190 1 - - Garcia-Gómez (2002)
170x200 1-2 130-135 - Sánchez-Tocinoetal.(2007)
240-453 1-2 141-210 8.04±0.13 CurrentStudy
90-120 - 85-100 13(20-22°C) Orteaetal.(1996)
90-120 1 - - Garcia-Gómez(2002)
170x200 1-2 130-135 - Sánchez-Tocinoetal.(2007)
85-181 1 71-90 7.71±0.17 CurrentStudy
300-400 - Bitsmallerthancapsules - Orteaetal.(1996)
320-360 1 - - Garcia-Gómez (2002)
300-599 1 173-430 28.00±0.82 CurrentStudy
ACKNOWLEDGMENTS
serve as first food for juveniles after
hatching(GibsonandChía, 1991).
Althoughsomeworkis stillrequired This work was carried out under a
to understand some of the differences research project funded by Prémio
here recognized in development pat- Milénio Sagres/Expresso 2002. R.C.
terns between these species, the data holds a grant from the Funda^áo para a
presented in this work with a systema- Ciencia e Tecnologia, Portugal (BDE
tised character and controlled hus- 15577/2005). Antonio Monteiro, and
bandry conditions of specimens, will Manuel Malaquias, read an early
certainly be useful regarding potential versión ofthe manuscript and helped to
taxonomicorphylogeneticdiscussions. improveit.
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